During April--July 2009, the Utah Department of Health identified five cases of Salmonella Typhimurium infection with indistinguishable pulsed-field gel electrophoresis (PFGE) patterns, predominantly among children. In August, CDC began a multistate outbreak investigation to determine the source of the infections. This report summarizes the results of this ongoing investigation, which, as of December 30, had identified 85 S. Typhimurium human isolates with the outbreak strain from 31 states. In a multistate case-control study, exposure to frogs was found to be significantly associated with illness (63% of cases versus 3% of controls; matched odds ratio [mOR] = 24.4). Among 14 case-patients who knew the type of frog, all had exposure to an exclusively aquatic frog species, the African dwarf frog. Environmental samples from aquariums containing aquatic frogs in four homes of case-patients yielded S. Typhimurium isolates matching the outbreak strain. Preliminary traceback information has indicated these frogs likely came from the same breeder in California. Reptiles (e.g., turtles) and amphibians (e.g., frogs) have long been recognized as Salmonella carriers (1,2), and three multistate outbreaks of human Salmonella infections associated with turtle contact have occurred since 2006 (3,4). However, this is the first reported multistate outbreak of Salmonella infections associated with amphibians. Educational materials aimed at preventing salmonellosis from contact with reptiles should be expanded to include amphibians, such as aquatic frogs.

The five cases identified in July 2009 by the Utah Department of Health all had isolates indistinguishable by pulsed field gel electrophoresis and were identified with XbaI pattern JPXX01.0177. The cases had occurred during April--July. On September 29, PulseNet, the national molecular subtyping network for foodborne disease surveillance, identified a national increase of isolates with this PFGE pattern (37 isolates from 19 states in 60 days). Multiple-locus variable-number tandem repeat analysis (MLVA) provided additional discrimination of the outbreak strain.For this investigation,a case was defined as S. Typhimurium infection with illness onset on or after April 1, 2009, with 1) PFGE pattern indistinguishable from the cluster-defining pattern and 2) MLVA pattern either matching that of the main outbreak strain, or MLVA unknown.

The multistate investigation began with in-depth, open-ended interviews of salmonellosis patients regarding exposures in the week before illness onset. A total of 11 interviews with patients were conducted through November. All 11 persons reported consumption of cheese-flavored crackers; eight reported exposure to aquatic animals, including fish and aquatic frogs.

As of December 30, 2009, S. Typhimurium isolates with the outbreak strain had been identified in 85 patients from 31 states, extending from Massachusetts to California, with week of illness onset ranging from March 22 to November 29 (Figure 1). Among the patients, 52% were male; median age was 5 years (range: 3 weeks--54 years), and 79% were aged <10 years. Among 47 patients with outcome information available, 16 (34%) had been hospitalized; no deaths were reported.

Case-Control Study

To examine possible associations between illness and consumption of cheese crackers and exposure to aquatic pets, CDC conducted a nationwide case-control study during November 30--December 7. Patients infected with S. Typhimurium with the outbreak strain who had specimen collection dates after July 15 were enrolled. Controls were persons with recent infection of Salmonella strains other than the outbreak strain and matched to case-patients by age and county of residence. Exposure histories were collected for 7 days before illness onset for case-patients and for 7 days before interview for controls.

Investigators sought to match each case-patient with two controls. A total of 19 case-patients (18 with stool specimens and one with a urine specimen) and 31 matching controls were enrolled from 15 states. Case-patients were found to be significantly more likely than controls to have had exposure to an aquatic pet, including fish and frogs (74% of case-patients versus 35% of controls; mOR = 4.7 [95% confidence interval (CI) = 1.2--27.0]). More specifically, illness was found to be associated with exposure to frogs (63% of case-patients versus 3% of controls; mOR = 24.4 [CI = 4.0--infinity]). Exposure to fish was not statistically significant (58% of case-patients versus 29% of controls, mOR = 3.1 [CI = 0.8--14.2]). No association was found between illness and consumption of any food item, including cheese crackers.

Among 39 patients interviewed as of December 9, including some of the 19 case-patients enrolled in the case-control study, 14 knew the type of frog involved in their exposure, and all 14 identified the frog as an African dwarf frog (Figure 2). When asked about potential for Salmonella infection, 19 of 36 (53%) patients reported awareness of association between contact with reptiles and Salmonella infection, but only 11 of 36 (31%) reported awareness of association with amphibians.* Among 20 patients from whom the information was available, the frog's aquarium was cleaned in the kitchen sink in the homes of six persons (30%) and in the bathroom sink in the homes of seven others (35%).

Environmental Testing and Traceback

Environmental samples taken from patient homes in four states yielded the outbreak strain of S. Typhimurium. The Colorado Department of Public Health obtained matched isolates from two African dwarf frogs, and from a rock and water in the aquarium containing the two frogs. The New Mexico Department of Health matched the outbreak strain with isolates from the filtration system, gravel, and water from an aquarium in a patient's home containing fish and a small water frog. The Ohio Department of Health matched the outbreak strain with isolates from a patient's deceased African dwarf frog, its water, and the lid and edge of its aquarium. The Utah Department of Health obtained matched isolates from a container used to clean African dwarf frogs in a patient's home.

Traceback investigations of frogs associated with positive environmental isolates have been completed. African dwarf frogs from the homes of the Colorado patient and the Utah patient were prizes from games at two different carnivals. The vendor who distributed the frogs to both carnivals was from Utah and identified the source as a breeder in California. Environmental sampling from the vendor's home (of aquarium filters and skin previously shed from African dwarf frogs) yielded multiple isolates matching the outbreak strain. The aquatic frog from the home of the New Mexico patient was purchased from a pet store chain, whose distributor identified the same breeder as the source for all of its aquatic frogs. The family of the Ohio patient purchased its African dwarf frog from a department store, whose distributor identified the breeder as the ultimate source of its frogs.

Environmental sampling from the breeder's California facility yielded S. Typhimurium isolates matching the outbreak strain. Positive samples were collected from multiple locations in the facility, including water tanks that contained African dwarf frogs and gravel in the water filtration system.

Editorial Note:

Salmonella illness remains a major public health problem in the United States, with an estimated 1.4 million human Salmonella infections, 15,000 hospitalizations, and 400 deaths annually (5). Although most Salmonella infections are foodborne, animal contact is an important source of human salmonellosis (6). Studies conducted during 1996--1997 determined that approximately 74,000 Salmonella infections each year in the United States resulted from reptile and amphibian exposure (1). The ongoing investigation described in this report documents the first multistate outbreak of Salmonella infections associated with amphibians. A case-control study described here found an association between infections and exposure to aquatic pet frogs such as African dwarf frogs. In addition, the outbreak strain was isolated from African dwarf frogs in two patient homes, from a container used to clean African dwarf frogs in a third home, and from water in an aquarium containing a small frog in a fourth home. Traceback investigations converged on a breeder in California; environmental sampling of the breeder's facility yielded the outbreak strain.

The most likely source of transmission in this outbreak was contact with water from the frogs' aquariums. Because African dwarf frogs are small and tend to rest at the bottom of aquariums where children have difficulty reaching them, direct handling as the source of transmission is less likely. Amphibians are known carriers of Salmonella (2). African dwarf frogs are purely aquatic animals, typically <2 inches long from nose to tail stub, and sold as ornamental aquarium pets. In one study, 21% of aquarium frogs tested from 16 retailers were positive for Salmonella (2). Furthermore, Salmonella bacteria shed from frogs are readily recoverable from aquarium water where frogs are housed (2). Salmonella can survive for an extended period in the environment, and indirect transmission through environmental contamination might occur (1).

Although 53% of case-patients described in this report knew that Salmonella infection could be acquired from reptiles, including turtles, only 31% knew that Salmonella could be acquired from amphibians. These findings are consistent with anecdotal reports of persons buying frogs as pets as an alternative to pet turtles because of concern over salmonellosis. Human exposure to Salmonella from aquariums can occur in homes, but also in pet stores, retail stores, schools, or child care centers (7). Public education regarding the risk for illness associated with turtles and other reptiles should be expanded to include the risk for salmonellosis from aquatic pet frogs and other amphibians. Most notably, because children aged <5 years might be less likely to consistently practice proper hand hygiene, prevention and control measures should be emphasized for this age group.

Water contained in aquariums where frogs and other amphibians are housed is an ideal environment for Salmonella growth (1,2,8). Aquarium water should be changed regularly and aquariums should be cleaned frequently. However, in this investigation, in 30% of patient households, aquariums were cleaned in the kitchen sink, posing a risk for cross-contamination with food preparation areas (2). CDC has published guidelines for consumers on how to reduce the risk for Salmonella infection from amphibians and reptiles (available at http://www.cdc.gov/salmonella/typh1209/index.html). Preventive measures include washing hands thoroughly with soap and water after touching animals or cleaning aquariums. No regulations prohibit the sale of small frogs, but education measures might help reduce the risk for Salmonella transmission.

* Persons interviewed included adult patients and parents or caretakers of children who were patients. They were asked: "Before this illness were you (or was your child) aware of any connection between reptile contact, such as contact with turtles or iguanas, and Salmonella?" and "Before this illness were you (or was your child) aware of any connection between amphibian contact, such as contact with frogs or salamanders, and Salmonella?"

What is already known on this topic?

Salmonella infection can be acquired through contact with reptiles and amphibians in homes, petting zoos, parks, child day care facilities, and other locations.

What is added by this report?

An ongoing multistate outbreak of human Salmonella infection has been associated with exposure to aquatic pet frogs; this is the first reported multistate salmonellosis outbreak associated with exposure to amphibians.

What are the implications for public health practice?

Longstanding salmonellosis education efforts targeting reptiles (e.g., pet turtles) should be expanded to include amphibians, and consumers should follow CDC guidelines for proper maintenance of aquariums.

FIGURE 1. Number (N = 83*) of cases of infection with the outbreak strain of Salmonella Tyhimurium, by week of illness onset† --- United States, 2009

* Reported as of December 30, 2009. Illnesses that began during the week of December 6 or later might not yet be reported. Two of 85 cases had no date for illness onset or isolation of organism from specimen and are not represented in this figure.

† Thirty-five illness onset dates were estimated from dates the outbreak strain was isolated from specimens.

Alternate Text: The figure above shows the number (N = 83) of cases of infection with the outbreak strain of Salmonella Tyhimurium, by week of illness onset during an outbreak in the United States in 2009. As of December 30, 2009, S. Typhimurium isolates with the outbreak strain had been identified in 85 patients from 31 states, extending from Massachusetts to California, with week of illness onset ranging from March 22 to November 29.

FIGURE 2. African dwarf frog

Photo/CDC

Alternate Text: The figure above shows an African dwarf frog.

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